Early cardiac morphogenesis is independent of function

Manasek, Francis J.; Monroe, R. Grier

doi:10.1016/0012-1606(72)90196-0

Cited by 69 publications

(44 citation statements)

References 6 publications

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“…Arresting myocardial contraction with potassium does not prevent looping (Manasek and Monroe, 1972). lowing:…”

Section: Previous Hypotheses For Loopingmentioning

confidence: 97%

“…Although several hypotheses have been proposed for looping, none have survived experimental scrutiny unscathed. It is generally accepted, however, that looping involves biomechanical forces, and many experiments have been designed to investigate these forces (Butler, 1952;Manasek and Monroe, 1972;Lacktis and Manasek, 1978;Manasek et al, 1978Manasek et al, , 1984aManasek, 1981;Icardo and Ojeda, 1984;Baldwin and Solursh, 1989;Manning and McLachlan, 1990;Itasaki et al, 1991).…”

Section: Introductionmentioning

confidence: 99%

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Mechanics of cardiac looping

Taber

Lin

Clark

1995

Developmental Dynamics

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During the early stages of embryonic development, the heart is a smoothwalled, muscle-wrapped tube that bends and rotates in a vital, but poorly understood, morphogenetic process called looping. Since looping involves biomechanical forces, this paper examines two mechanically based hypotheses for the bending component of cardiac looping. The first hypothesis is that an initial tension in or near the dorsal mesocardium (DM), a longitudinal structure along the outside of the ventricle, drives the deformation. To relieve the bending stresses in the tube, the myocytes change shape passively, and then they deform actively to continue the process to completion of a full loop. In the second hypothesis, contraction of circumferentially arranged actin macrofilaments produces circumferential compression and longitudinal expansion (due to incompressibility) of the myocytes. The DM locally constrains the longitudinal deformation, forcing the tube to bend. The feasibility of these hypotheses was evaluated using theoretical models and published experimental results. The models, which consist of beams composed of two layers representing the DM and the ventricular myocardium, show that the hypotheses are consistent with most of the known data, but further studies are necessary. In this regard, the models provide a conceptual framework for designing experiments to investigate the mechanics of looping. 0 1995 Wiley-Liss, Inc.

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“…Arresting myocardial contraction with potassium does not prevent looping (Manasek and Monroe, 1972). lowing:…”

Section: Previous Hypotheses For Loopingmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 99%

Mechanics of cardiac looping

Taber

Lin

Clark

1995

Developmental Dynamics

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“…Because heartbeat is not required for looping to occur, 11,17 only cytoskeletal contraction is included in our model. For both MY and CJ, the passive strain-energy density function was taken in the form…”

Section: Materials Propertiesmentioning

confidence: 99%

“…Since the heartbeat does not affect looping, 11,17 functional strains were eliminated by temporarily stopping the heart by cooling the culture dish and embryo in an ice bath. Studies in our laboratory have shown that the heart stops beating within several minutes of cooling, and development proceeds normally once the embryo is re-warmed.…”

Section: Tissue Labelingmentioning

confidence: 99%

Computational Model for Early Cardiac Looping

et al. 2006

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Abstract-Looping is a vital event during early cardiac morphogenesis, as the initially straight heart tube bends and twists into a curved tube, laying out the basic pattern of the future fourchambered heart. Despite intensive study for almost a century, the biophysical mechanisms that drive this process are not well understood. To explore a recently proposed hypothesis for looping, we constructed a finite element model for the embryonic chick heart during the first phase of looping, called c-looping. The model includes the main structures of the early heart (heart tube, omphalomesenteric veins, and dorsal mesocardium), and the analysis features realistic three-dimensional geometry, nonlinear passive and active material properties, and anisotropic growth. As per our earlier hypothesis for c-looping, actin-based morphogenetic processes (active cell shape change, cytoskeletal contraction, and cell migration) are simulated in specific regions of the model. The model correctly predicts the initial gross morphological shape changes of the heart, as well as distributions of morphogenetic stresses and strains measured in embryonic chick hearts. The model was tested further in studies that perturbed normal cardiac morphogenesis. The model, taken together with the new experimental data, supports our hypothesis for the mechanisms that drive early looping.

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“…The "flow-molding" hypothesis, in which centrifugal forces generated by blood flowing through the forming heart were presumed responsible for shaping the cardiac chambers, gained early favor (Roux 1895;Spitzer 1923) and was still cited many decades later (e.g., Stalsberg 1970). Perhaps the most definitive test of the flow-molding hypothesis in the tube heart stage was by Manasek and Monroe (1972), who observed that explanted, nonbeating, but otherwise intact embryonic chicken hearts grown from HH stages 9-12 in vitro still showed typical patterns of cardiac looping. Variations on these experiments have been repeated with similar outcomes on numerous occasions (see review by Manasek 1983;Manning and McLachlan 1990).…”

Section: Cardiac Morphogenesismentioning

confidence: 99%

What Is the Purpose of the Embryonic Heart Beat? or How Facts Can Ultimately Prevail over Physiological Dogma

Burggren

2004

Physiological and Biochemical Zoology

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Embryonic physiology is often viewed as merely those processes understood for the adult but conducted on a smaller physical scale. Yet striking examples of the inaccuracy of this perspective can be identified in the embryonic cardiovascular system. For example, dogma holds that the embryonic heart begins to beat to pump blood for convective transport, just like that of the adult. This is the major assumption inherent in the hypothesis we have called "convective synchronotropy"; that is, the embryonic heart starts to beat synchronously with the need for convective blood flow. However, there is compelling evidence on many fronts that the convective flow of blood generated by the early embryonic vertebrate heart is simply not required for transport of oxygen, nutrients, metabolic wastes, or hormones, all of which can be achieved entirely by diffusion. In fact, fish, amphibian, and bird embryos lacking a functional heart (either through surgical intervention or mutation) or whose oxygenhemoglobin transport has been chemically eliminated nonetheless continue to function and grow in size for extended periods up to the point at which diffusion alone can no longer serve oxygen transport needs. We advocate the alternative hypothesis of "prosynchronotropy" (i.e., the heart starts to beat well before convective blood flow is needed for bulk transport). So, what is the purpose of the early embryonic heart beat? Evidence is presented herein in support of a morphogenic rationale for prosynchronotropy. Specifically, it appears that the initial rationale for the beat of the vertebrate embryonic heart may be two-fold: to aid in subtle but significant aspects of cardiac growth, shaping, and maturation, and to facilitate cardiac maturation angiogenesis-the formation of new vessels by sprouting from vessel tips. Ultimately, the embryonic cardio-*

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Early cardiac morphogenesis is independent of function

Cited by 69 publications

References 6 publications

Mechanics of cardiac looping

Mechanics of cardiac looping

Computational Model for Early Cardiac Looping

What Is the Purpose of the Embryonic Heart Beat? or How Facts Can Ultimately Prevail over Physiological Dogma

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